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Fe0 nanoparticles improve physiological and antioxidative attributes of sunflower (Helianthus annuus) plants grown in soil spiked with hexavalent chromium

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Abstract

Contamination of agricultural land by chromium (Cr) can inhibit physiological and biochemical processes in plants, leading to reduced crop productivity and food/feed safety. Owing to their fine size, large surface area, and high adsorption affinity for metals, nanomaterials have shown a potential for phytoremediation of heavy metal-contaminated soils. Nanomaterials enhance fitness of plants under metal stress through their modifying effects on plant physiology and biochemistry. The aim of this study was to assess the performance of sunflower (Helianthus annuus) plants grown in soil spiked with hexavalent chromium (Cr IV; 0, 75 and 150 ppm) and the potential role of nano-zerovalent iron (Fe0 nanoparticles; 0, 1 and 2%) to ameliorate Cr toxicity. Results revealed that the Cr uptake decreased by increasing the concentration of Fe0 nanoparticles, causing a significant enhancement in plant morphological and physiological attributes. Treatment with Fe0 nanoparticles reduced bioaccumulation factor (BAF) (in both root and shoot tissues) and translocation factor (TF); however, the magnitude of BAF and TF decreased significantly by increasing the level of Cr(VI). Chromium stress increased the activities of antioxidant enzymes, which further increased by Fe0 nanoparticle application, resulting in improved growth traits. A significant positive correlation was found between growth, BAF and TF of seedlings treated with Fe0 nanoparticles (both 1 and 2%) upon Cr exposure (75 and 150 ppm). The results demonstrated the potential of Fe0 nanoparticles to improve performance of sunflower plants under Cr toxicity through reducing their Cr uptake, which was accompanied by enhanced activity of detoxification enzymes (SOD, CAT, POX, and APX) in cells.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Bai P, Zeng F, Cai S, Shamsi IH, Qiu B, Wu F, Zhang G (2011) The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance. Environ Exp Bot 70(2):185–191

    Article  CAS  Google Scholar 

  • Alia Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200

    Article  CAS  PubMed  Google Scholar 

  • Amin H, Arain BA, Amin F, Surhio MA (2013) Phytotoxicity of chromium on germination, growth and biochemical attributes of Hibiscus esculentus L. Am J Plant Sci 4:2431–2439

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Asgari Lajayer B, Ghorbanpour M, Nikabadi S (2017a) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol Environ Saf 145:377–390

    Article  CAS  PubMed  Google Scholar 

  • Asgari Lajayer H, Savaghebi G, Hadian J, Hatami M, Pezhmanmehr M (2017b) Comparison of copper and zinc effects on growth, micro and macronutrients status and essential oil constituents in pennyroyal (Mentha pulegium L.). Braz J Bot 40:379–388

    Article  Google Scholar 

  • Asgari LB, Khadem Moghadam N, Maghsoodi MR, Ghorbanpour M, Kariman Kh (2019) Phytoextraction of heavy metals from contaminated soil, water and atmosphere using ornamental plants: mechanisms and efficiency improvement strategies. Environ Sci Pollut Res 26:8468

    Article  CAS  Google Scholar 

  • Baiazidi-Aghdam MT, Mohammadi H, Ghorbanpour M (2016) Effects of nanoparticulate anatase titanium dioxide on physiological and biochemical performance of Linum usitatissimum (Linaceae) under well watered and drought stress conditions. Braz J Bot 39:139–146

    Article  Google Scholar 

  • Barnhart N (1997) Chromium and its soils in the proximity of the old tannery waste lagoon. Int Agrophys 15:121–124

    Google Scholar 

  • Barton LL, Johnson AG, Wagener BM (2000) Inhibition of ferric chelate reductase in alfalfa roots by cobalt, nickel, chromium and copper. J Plant Nutr 23:1833–1845

    Article  CAS  Google Scholar 

  • Bhowmick S, Chakraborty S, Mondal P, Van Renterghem W, Van den Berghe S, Roman-Ross G, Chatterjee D, Iglesias M (2014) Montmorillonite-supported nanoscale zero-valent iron removal of arsenic from aqueous solution: kinetics and mechanism. Chem Eng J 243:14–23

    Article  CAS  Google Scholar 

  • Bishnoi NR, Chugh LK, Sawhney SK (1993) Effect of chromium on photosynthesis, respiration and nitrogen fixation in pea (Pisum sativum L.) seedlings. J Plant Physiol 142:25–30

    Article  CAS  Google Scholar 

  • Borowiak K, Drzewiecka K, Magdziak Z, Gasecka M, Mleczek M (2012) Effect of Ca/Mg ions ratio on copper accumulation, photosynthetic activity and growth of Cu2+-treated Salix viminalis L. ‘Cannabina’. Photosynthetica 50:353. https://doi.org/10.1007/s11099-012-0040-8

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Brooks RR (1998) Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining. CAB International, Wallingford, p 380

    Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Cohen MD, Kargacin B, Klein CB, Costa M (1993) Mechanism of chromium carcinogenicity and toxicity. Crit Rev Toxicol 23:255–281

    Article  CAS  PubMed  Google Scholar 

  • Dhindsa RS, Dhindsa PP, Thorpe TA (1980) Leaf senescence correlated with increased levels of membrane permeability and lipid-peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  Google Scholar 

  • Forte J, Mutiti S (2017) Phytoremediation potential of Helianthus annuus and Hydrangea paniculata in copper and lead-contaminated soil. Water Air Soil Pollut 228:1–11

    Article  CAS  Google Scholar 

  • Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49

    Article  CAS  PubMed  Google Scholar 

  • Ghorbanpour M, Hadian J (2015) Multi-walled carbon nanotubes stimulate callus induction, secondary metabolites biosynthesis and antioxidant capacity in medicinal plant Satureja khuzestanica grown in vitro. Carbon 94:749–759

    Article  CAS  Google Scholar 

  • Ghorbanpour M, Hatami H (2015) Changes in growth, antioxidant defense system and major essential oils constituents of Pelargonium graveolens plant exposed to nano-scale silver and thidiazuron. Ind J Plant Physiol. 20(2):116–123

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatami M, Hosseini SM, Ghorbanpour M, Kariman K (2019) Physiological and antioxidative responses to GO/PANI nanocomposite in intact and demucilaged seeds and young seedlings of Salvia mirzayanii. Chemosphere 233:920–935

    Article  CAS  PubMed  Google Scholar 

  • Houben D, Sonnet P (2010) Leaching and phytoavailability of zinc and cadmium in a contaminated soil treated with zero-valent iron. In: Proceedings of the 19th world congress of soil science, soil solutions for a changing world, pp 1–6

  • Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot Rev 75:339–364

    Article  Google Scholar 

  • Janas KM, Zieli A, Ska-Tomaszewska J, Rybaczek D, Maszewski J, Posmyk MM, Amarowicz R, Kosińska A (2010) The impact of copper ions on growth, lipid peroxidation, and phenolic compound accumulation and localization in lentil (Lens culinaris Medic.) seedlings. J Plant Physiol 167:270–276

    Article  CAS  PubMed  Google Scholar 

  • Juwarkar AA, Singh SK, Mudhoo A (2010) A comprehensive overview of elements in bioremediation. Rev Environ Sci Biotechnol 9:215–288

    Article  CAS  Google Scholar 

  • Kumar NP, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  PubMed  Google Scholar 

  • Ladislas S, El-Mufleh A, Gerente C, Chazarenc F, Andres Y, Bechet B (2012) Potential of aquatic macrophytes as bioindicators of heavy metal pollution in urban stormwater runoff. Water Air Soil Pollut 223:877–888

    Article  CAS  Google Scholar 

  • Liang D, Wang B, Song S, Wang J, Wang L, Ren X, Zhao X (2019) Analysis of genetic effects on a complete diallel cross test of Pinus koraiensis. Euphytica 215(5):92

    Article  Google Scholar 

  • Liu JH, Inoue H, Moriguchi T (2008) Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots. Environ Exp Bot 62:28–35

    Article  CAS  Google Scholar 

  • Macnair MR, Tilstone GH, Smith SE (2000) The genetics of metal tolerance and accumulation in higher plants. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, pp 235–250

    Google Scholar 

  • Maiti S, Ghosh N, Mandal C, Das K, Dey N, Adak MK (2012) Responses of the maize plant to chromium stress with reference to antioxidation activity. Braz J Plant Physiol 24(3):203–212

    Article  CAS  Google Scholar 

  • Malik JA, Kumar S, Thakur P, Sharma S, Kaur N, Kaur R, Pathania D, Bhandhari K, Kaushal N, Singh K, Srivastava A (2011) Promotion of growth in mungbean (Phaseolus aureus Roxb.) by selenium is associated with stimulation of carbohydrate metabolism. Biol Trace Elem Res 143(1):530–539

    Article  CAS  PubMed  Google Scholar 

  • Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H (2012) Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot 77:242–248

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  • Mehta SK, Gaur JP (1999) Heavy metal induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Physiol 143:253–259

    Article  CAS  Google Scholar 

  • Mohammadi H, Hatami M, Feghezadeh K, Ghorbanpour M (2018) Mitigating effect of nano-zerovalent iron, iron sulfate and EDTA against oxidative stress induced by chromium in Helianthus annuus L. Acta Physiol Plant 40:69

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867

    CAS  Google Scholar 

  • Nasiri J, Gholami A, Panahpour E (2013) Removal of cadmium from soil resources using stabilized zero-valent iron nanoparticles. J Civ Eng Urban 3:338–341

    Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Obrouchova NV, Bystrova EI, Ivanov VB, Anupova O, Seregin I (1998) Root growth responses to lead in young maize seedlings. Plant Soil 200:55–61

    Article  Google Scholar 

  • Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Water Air Soil Pollut 184:105–126

    Article  CAS  Google Scholar 

  • Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol 17:95–192

    Article  CAS  Google Scholar 

  • Piechalak A, Tomaszewska B, Barałkiewicz D, Malecka A (2002) Accumulation and detoxification of lead in legumes. Phytochemistry 60:153–162

    Article  CAS  PubMed  Google Scholar 

  • Poguberović SS, Krčmar DM, Maletić SP, Kónya Z, Pilipović DD, Kerkez DV, Rončević SD (2016) Removal of As (III) and Cr(VI) from aqueous solutions using “green” zero-valent iron nanoparticles produced by oak, mulberry and cherry leaf extracts. Ecol Eng 90:42–49

    Article  Google Scholar 

  • Prasad MNV, Strzaka K (2002) Physiology and biochemistry of metal toxicity and tolerance in plants. Plant Sci 161:881–889

    Article  Google Scholar 

  • Qu X, Alvarez PJ, Li Q (2013) Applications of nanotechnology in water and wastewater treatment. Water Res 47:3931–3946

    Article  CAS  PubMed  Google Scholar 

  • Radojevic M, Bashkin VN (1999) Practical environmental analysis. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Sandmann G, Böger P (1980) Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol 66:797–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shanker KA, Cervantes C, Loza-Taversa H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Abid AD, Kennedy IM, Hristova KR, Silk WK (2011) To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution. Environ Pollut 159:1277–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh J, Lee BK (2016) Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max): a possible mechanism for the removal of Cd from the contaminated soil. J Environ Manag 170:88–96

    Article  CAS  Google Scholar 

  • Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11(3):229–254

    Article  CAS  Google Scholar 

  • Song J, Zhang H, Duan C, Cui X (2018) Exogenous application of succinic acid enhances tolerance of Larix olgensis seedling to lead stress. J For Res 29(6):1497–1505

    Article  CAS  Google Scholar 

  • Sun RL, Zhou QX, Jin CX (2006) Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Plant Soil 285:125–134

    Article  CAS  Google Scholar 

  • Sundaramoorthy P, Alagappan C, Kaliyaperumal SG, Pachikkaran U, Logalashmanan B (2010) Chromium stress in paddy: (i) nutrient status of paddy under chromium stress; (ii) phytoremediation of chromium by aquatic and terrestrial weeds. CR Biol 333:597–607

    Article  CAS  Google Scholar 

  • Tafazoli M, Hojjati SM, Biparva P, Kooch Y, Lamersdorf N (2017) Reduction of soil heavy metal bioavailability by nanoparticles and cellulosic wastes improved the biomass of tree seedlings. J Plant Nutr Soil Sci 180:683–693

    Article  CAS  Google Scholar 

  • Tian H, Ghorbanpour M, Kariman K (2018) Manganese oxide nanoparticle-induced changes in growth, redox reactions and elicitation of antioxidant metabolites in deadly nightshade (Atropa belladonna L.). Ind Crops Prod 126:403–414

    Article  CAS  Google Scholar 

  • Tripathi DK, Singh VP, Prasad SM, Chauhan DK, Dubey NK, Rai AK (2015) Silicon-mediated alleviation of Cr(VI) toxicity in wheat seedlings as evidenced by chlorophyll florescence, laser induced breakdown spectroscopy and anatomical changes. Ecotoxicol Environ Saf 113:133–144

    Article  CAS  PubMed  Google Scholar 

  • Tucker M (1974) A modified heating block foe plant tissue digestion 1. Commun Soil Sci Plant Anal 5:539–546

    Article  Google Scholar 

  • Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17

    Article  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effect of metal on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Verma S, Dubey R (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    Article  CAS  Google Scholar 

  • Vilardi G, Verdone N, Di Palma L (2017) The influence of nitrate on the reduction of hexavalent chromium by zero-valent iron nanoparticles in polluted wastewater. Desalin Water Treat 86:252–258

    Article  CAS  Google Scholar 

  • Wang C, Luo H, Zhang Z, Wu Y, Zhang J, Chen S (2014) Removal of As(III) and As(V) from aqueous solutions using nanoscale zero valent iron-reduced graphite oxide modified composites. J Hazard Mater 268:124–131

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Murata Y, Nakamura T, Sakai Y, Osaki M (2009) Effect of zero-valent iron application on cadmium uptake in rice plants grown in cadmium-contaminated soils. J Plant Nutr 32:1164–1172

    Article  CAS  Google Scholar 

  • Zayed A, Lytle CM, Jin-Hong Q, Terry N, Qian JH (1998) Chromium accumulation, translocation and chemical speciation in vegetable crops. Planta 206:293–299

    Article  CAS  Google Scholar 

  • Zenk M (1996) Heavy metal deteoxification. Curr Opin Plant Biol 3:211–216

    Google Scholar 

  • Zhuang P, Yang Q, Wang H, Shu W (2007) Phytoextraction of heavy metals by eight plant species in the field. Water Air Soil Pollut 184:235–242

    Article  CAS  Google Scholar 

  • Zu YQ, Li Y, Chen JJ, Chen HY, Qin L, Schvartz C (2005) Hyperaccumulation of Pb, Zn and Cd in herbaceous plants grown on lead–zinc mining area in Yunnan, China. Environ Int 31:755–762

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by Deputy of Research and Technology of Azarbaijan Shahid Madani University (95/D/897), Tabriz, Iran.

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Authors and Affiliations

  1. Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran

    Hamid Mohammadi

  2. Applied Chemistry Research Laboratory, Department of Chemistry, Faculty of Basic Science, Azarbaijan Shahid Madani University (ASMU), Tabriz, 53751-71379, Iran

    Ali Reza Amani-Ghadim

  3. Department of Chemistry, Faculty of Basic Science, Azarbaijan Shahid Madani University (ASMU), Tabriz, 53751-71379, Iran

    Amir Abbas Matin

  4. Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, 38156‑8‑8349, Iran

    Mansour Ghorbanpour

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  1. Hamid Mohammadi
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Mohammadi, H., Amani-Ghadim, A.R., Matin, A.A. et al. Fe0 nanoparticles improve physiological and antioxidative attributes of sunflower (Helianthus annuus) plants grown in soil spiked with hexavalent chromium. 3 Biotech 10, 19 (2020). https://doi.org/10.1007/s13205-019-2002-3

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